A Phytophthora Effector Suppresses Trans-Kingdom RNAi to Promote Disease Susceptibility

• Published in: Cell host & microbe Vol. 25; no. 1; pp. 153 - 165.e5
• Main Authors: Hou, Yingnan, Zhai, Yi, Feng, Li, Karimi, Hana Z., Rutter, Brian D., Zeng, Liping, Choi, Du Seok, Zhang, Bailong, Gu, Weifeng, Chen, Xuemei, Ye, Wenwu, Innes, Roger W., Zhai, Jixian, Ma, Wenbo
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 09.01.2019
• Subjects: Arabidopsis; Arabidopsis - genetics; Arabidopsis - immunology; Arabidopsis - microbiology; Arabidopsis Proteins - genetics; biogenesis; disease susceptibility; Disease Susceptibility - microbiology; Gene Expression Regulation, Plant; Gene Silencing; genes; Genes, Reporter - genetics; host-induced gene silencing; Host-Pathogen Interactions - genetics; Host-Pathogen Interactions - immunology; immunity; microRNA; MicroRNAs - genetics; MicroRNAs - immunology; Nicotiana; pathogenesis; pathogens; Phosphoprotein Phosphatases - antagonists & inhibitors; Phosphoprotein Phosphatases - metabolism; Phytophthora; Phytophthora - metabolism; Phytophthora - pathogenicity; Plant Diseases - immunology; Plant Diseases - microbiology; plant immunity; Plant Immunity - genetics; Plant Immunity - immunology; Plant Leaves - immunology; Plant Leaves - microbiology; RNA interference; RNA Interference - immunology; RNA, Small Interfering - biosynthesis; RNA, Small Interfering - drug effects; RNA, Small Interfering - genetics; RNA-Binding Proteins - genetics; RNA-Binding Proteins - metabolism; RNA-silencing suppressor; secondary small RNAs; Verticillium; Virulence; virulence factor; Virulence Factors - genetics; Virulence Factors - metabolism; pathogenesis; RNA interference; RNA-silencing suppressor; microRNA; host-induced gene silencing; secondary small RNAs; virulence factor; plant immunity
• ISSN: 1931-3128; 1934-6069; 1934-6069
• DOI: 10.1016/j.chom.2018.11.007

RNA silencing (RNAi) has a well-established role in anti-viral immunity in plants. The destructive eukaryotic pathogen Phytophthora encodes suppressors of RNAi (PSRs), which enhance plant susceptibility. However, the role of small RNAs in defense against eukaryotic pathogens is unclear. Here, we show that Phytophthora infection of Arabidopsis leads to increased production of a diverse pool of secondary small interfering RNAs (siRNAs). Instead of regulating endogenous plant genes, these siRNAs are found in extracellular vesicles and likely silence target genes in Phytophthora during natural infection. Introduction of a plant siRNA in Phytophthora leads to developmental deficiency and abolishes virulence, while Arabidopsis mutants defective in secondary siRNA biogenesis are hypersusceptible. Notably, Phytophthora effector PSR2 specifically inhibits secondary siRNA biogenesis in Arabidopsis and promotes infection. These findings uncover the role of siRNAs as antimicrobial agents against eukaryotic pathogens and highlight a defense/counter-defense arms race centered on trans-kingdom gene silencing between hosts and pathogens. [Display omitted] •Phytophthora infection increases production of a pool of secondary siRNAs in Arabidopsis•Secondary siRNAs from a PPR gene cluster contribute to defense against Phytophthora•PPR-siRNAs potentially silence Phytophthora transcripts to confer resistance•Phytophthora effector PSR2 suppresses the biogenesis of PPR-siRNAs to promote infection The role of plant RNAi in defense against eukaryotic pathogens is unclear. Hou et al. report that Arabidopsis produces a reservoir of secondary siRNAs that confer resistance against the notorious pathogen Phytophthora, likely through trans-kingdom gene silencing. However, a Phytophthora effector defeats this defense by specifically inhibiting secondary siRNA biogenesis.